Phosphorylation of dystrophin Dp71d by Ca2+/calmodulin-dependent protein kinase II modulates the Dp71d nuclear localization in PC12 cells

Journal of Neurochemistry

Volumn 98, Issue 3, 2006, Pages 713-722

  Calderilla Barbosa, Luis ^a   Ortega, Arturo ^a   Cisneros, Bulmaro ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

CaMKII; Dp71d; Dystrophin; Nuclear localization; PC12 cells; Phosphorylation

Indexed keywords

1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; BISINDOLYLMALEIMIDE; BISINDOLYLMALEIMIDE 1; DIACYLGLYCEROL KINASE INHIBITOR; DYSTROPHIN; EGTAZIC ACID; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN DERIVATIVE; PROTEIN DP71D; PROTEIN KINASE; PROTEIN KINASE (CALCIUM,CALMODULIN) II; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; SERINE; THREONINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL LINE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; DEPOLARIZATION; EXPRESSION VECTOR; NONHUMAN; NUCLEAR IMPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL NUCLEUS; DYSTROPHIN; NUCLEAR LOCALIZATION SIGNALS; PC12 CELLS; PHOSPHORYLATION; RATS;

EID: 33745927712     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03904.x     Document Type: Article

References (41)

1. Acosta R., Montanez C., Fuentes-Mera L., Gonzalez E., Gomez P., Quintero-Mora L., Mornet D., Alvarez-Salas L. M. and Cisneros B. (2004) Dystrophin Dp71 is required for neurite outgrowth in PC12 cells. Exp. Cell Res. 296, 265-275.
2. Ahn A. H. and Kunkel L. M. (1993) The structural and functional diversity of dystrophin. Nat. Genet. 3, 283-291.
3. Austin R. C., Howard P. L., D'Souza V. N., Klamut H. J. and Ray P. N. (1995) Cloning and characterization of alternatively spliced isoforms of Dp71. Hum. Mol. Genet. 4, 1475-1483.
4. Bar S., Barnea E., Levy Z., Neuman S., Yaffe D. and Nudel U. (1990) A novel product of the Duchenne muscular dystrophy gene which greatly differs from the known isoforms in its structure and tissue distribution. Biochem. J. 272, 557-560.
5. Blake D. J. and Kroger S. (2000) The neurobiology of duchenne muscular dystrophy: learning lessons from muscle? Trends Neurosci. 23, 92-99.
6. Blake D. J., Weir A., Newey S. E. and Davies K. E. (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev. 82, 291-329.
7. Boyce F. M., Beggs A. H., Feener C. and Kunkel L. M. (1991) Dystrophin is transcribed in brain from a distant upstream promoter. Proc. Natl Acad. Sci. USA 88, 1276-1280.
8. Byers T. J., Lidov H. G. and Kunkel L. M. (1993) An alternative dystrophin transcript specific to peripheral nerve. Nat. Genet. 4, 77-81.
9. Cisneros B., Rendon A., Genty V., Aranda G., Marquez F., Mornet D. and Montanez C. (1996) Expression of dystrophin Dp71 during PC12 cell differentiation. Neurosci. Lett. 213, 107-110.
10. D'Souza V. N., Nguyen T. M., Morris G. E., Karges W., Pillers D. A. and Ray P. N. (1995) A novel dystrophin isoform is required for normal retinal electrophysiology. Hum. Mol. Genet. 4, 837-842.
11. Davison M. D. and Critchley D. R. (1988) alpha-Actinins and the DMD protein contain spectrin-like repeats. Cell 52, 159-160.
12. Dupont J.-L., Janoshazi A., Bellahcene M., Mykita S. and de Barry J. (2000) Reversible protein kinase C activation in PC12 cells: effect of NGF treatment. Eur. J. Neurosci. 12, 215-226.
13. Enriquez-Aragon J. A., Cerna-Cortes J., Bermudez de Leon M., Garcia-Sierra F., Gonzalez E., Mornet D. and Cisneros B. (2005) Dystrophin Dp71 in PC12 cell adhesion. Neuroreport 16, 235-238.
14. Ervasti J. M. and Campbell K. P. (1991) Membrane organization of the dystrophin-glycoprotein complex. Cell 66, 1121-1131.
15. Fabbrizio E., Nudel U., Hugon G., Robert A., Pons F. and Mornet D. (1994) Characterization and localization of a 77 kDa protein related to the dystrophin gene family. Biochem. J. 299, 359-365.
16. Gonzalez E., Montanez C., Ray P. N., Howard P. L., Garcia-Sierra F., Mornet D. and Cisneros B. (2000) Alternative splicing regulates the nuclear or cytoplasmic localization of dystrophin Dp71. FEBS Lett. 482, 209-214.
17. Gorecki D. C. and Barnard E. A. (1995) Specific expression of G-dystrophin (Dp71) in the brain. Neuroreport 6, 893-896.
18. Gorecki D., Geng Y., Thomas K., Hunt S. P., Barnard E. A. and Barnard P. J. (1991) Expression of the dystrophin gene in mouse and rat brain. Neuroreport 2, 773-776.
19. Hoffman E. P., Kunkel L. M. and Brown R. H. Jr (1988) Proteolytic fragment or new gene product? Nature 336, 210.
20. Hugnot J. P., Gilgenkrantz H., Vincent N., Chafey P., Morris G. E., Monaco A. P., Berwald-Netter Y., Koulakoff A., Kaplan J. C., Kahn A. et al. (1992) Distal transcript of the dystrophin gene initiated from an alternative first exon and encoding a 75-kDa protein widely distributed in nonmuscle tissues. Proc. Natl Acad. Sci. USA 89, 7506-7510.
21. Kaffman A. and O'Shea E. K. (1999) Regulation of nuclear localization: a key to a door. Ann. Rev. Cell Dev. Biol. 15, 291-339.
22. Kau T. R., Way J. C. and Silver P. A. (2004) Nuclear transport and cancer: from mechanism to intervention. Nat. Rev. Cancer 4, 106-117.
23. Koenig M., Monaco A. P. and Kunkel L. M. (1988) The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53, 219-226.
24. Kutcher L. W., Beauman S. R., Gruenstein E. I., Kaetzel M. A. and Dedman J. R. (2003) Nuclear CaMKII inhibits neuronal differentiation of PC12 cells without affecting MAPK or CREB activation. Am. J. Physiol. 284, C1334-C1345.
25. Lapidos K. A., Kakkar R. and McNally E. M. (2004) The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ. Res. 94, 1023-1031.
26. Lidov H. G., Selig S. and Kunkel L. M. (1995) Dp140: a novel 140 kDa CNS transcript from the dystrophin locus. Hum. Mol. Genet. 4, 329-335.
27. Loh N. Y., Nebenius-Oosthuizen D., Blake D. J., Smith A. J. and Davies K. E. (2001) Role of beta-dystrobrevin in nonmuscle dystrophin-associated protein complex-like complexes in kidney and liver. Mol. Cell Biol. 21, 7442-7448.
28. Luise M., Presotto C., Senter L., Betto R., Ceoldo S., Furlan S., Salvatori S., Sabbadini R. A. and Salviati G. (1993) Dystrophin is phosphorylated by endogenous protein kinases. Biochem. J. 293, 243-247.
29. Madhavan R. and Jarrett H. W. (1994) Calmodulin-activated phosphorylation of dystrophin. Biochemistry 33, 5797-5804.
30. Madhavan R. and Jarrett H. W. (1999) Phosphorylation of dystrophin and alpha-syntrophin by Ca (2+)-calmodulin dependent protein kinase II. Biochim. Biophys. Acta 1434, 260-274.
31. Marquez F. G., Cisneros B., Garcia F., Ceja V., Velazquez F., Depardon F., Cervantes L., Rendon A., Mornet D., Rosas-vargas H., Mustre M. and Montanez C. (2003) Differential expression and subcellular distribution of dystrophin Dp71 isoforms during differentiation process. Neuroscience 118, 957-966.
32. Matthews R. P., Guthrie C. R., Wailes L. M., Zhao X., Means A. R. and McKnight G. S. (1994) Calcium/calmodulin-dependent protein kinase types II and IV differentially regulate CREB-dependent gene expression. Mol. Cell Biol. 14, 6107-6116.
33. Michalak M., Fu S. Y., Milner R. E., Busaan J. L. and Hance J. E. (1996) Phosphorylation of the carboxyl-terminal region of dystrophin. Biochem. Cell Biol. 74, 431-437.
34. Milner R. E., Busaan J. L., Holmes C. F., Wang J. H. and Michalak M. (1993) Phosphorylation of dystrophin. The carboxyl-terminal region of dystrophin is a substrate for in vitro phosphorylation by p34cdc2 protein kinase. J. Biol. Chem. 268, 21 901-21 905.
35. Petrof B. J., Shrager J. B., Stedman H. H., Kelly A. M. and Sweeney H. L. (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl Acad. Sci. USA 90, 3710-3714.
36. Senter L., Ceoldo S., Petrusa M. M. and Salviati G. (1995) Phosphorylation of dystrophin: effects on actin binding. Biochem. Biophys. Res. Commun. 206, 57-63.
37. Shemanko C. S., Sanghera J. S., Milner R. E., Pelech S. and Michalak M. (1995) Phosphorylation of the carboxyl terminal region of dystrophin by mitogen-activated protein (MAP) kinase. Mol. Cell Biochem. 152, 63-70.
38. Suzuki A., Yoshida M., Yamamoto H. and Ozawa E. (1992) Glycoprotein-binding site of dystrophin is confined to the cysteine-rich domain and the first half of the carboxy-terminal domain. FEBS Lett. 308, 154-160.
39. Tommasi di Vignano A., Di Zenzo G., Sudol M., Cesareni G. and Dente L. (2000) Contribution of the different modules in the utrophin carboxy-terminal region to the formation and regulation of the DAP complex. FEBS Lett. 471, 229-234.
40. Walsh M. P., Busaan J. L., Fraser E. D., Fu S. Y., Pato M. D. and Michalak M. (1995) Characterization of the recombinant C-terminal domain of dystrophin: phosphorylation by calmodulin-dependent protein kinase II and dephosphorylation by type 2B protein phosphatase. Biochemistry 34, 5561-5568.
41. Yoshida M. and Ozawa E. (1990) Glycoprotein complex anchoring dystrophin to sarcolemma. J. Biochem. (Tokyo) 108, 748-752.